Download PDF
Semin Reprod Med 2000; 18(3): 321-326
DOI: 10.1055/s-2000-12569
Copyright © 2000 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

The Placenta Dilemma

Susan J. Fisher
  • Departments of Stomatology; Obstetrics, Gynecology and Reproductive Sciences; Anatomy; and Pharmaceutical Chemistry and the Biomedical Sciences Graduate Program, University of California San Francisco, San Francisco, California
Further Information

Publication History

Publication Date:
31 December 2000 (online)

    Permissions and Reprints

ABSTRACT

Despite the critical role the placenta plays in governing the outcome of pregnancy, a great deal remains to be learned about this transient organ. Several factors have contributed to our relative lack of knowledge. For example, most of the placenta's development, which precedes that of the embryo or fetus, occurs during the first half of pregnancy in humans. Thus, it is difficult to obtain the tissue samples that are required to study relevant time points. In addition, placental anatomy is complex; one of the most interesting parts can be obtained only by biopsy of the uterine wall. Recent analyses of these biopsies, combined with information from cell culture models, revealed the unexpected finding that placental cells that invade the uterus phenocopy many endothelial cell characteristics. This finding has several interesting implications for normal pregnancy and for pregnancy complications that could be related, either directly or indirectly, to this phenomenon, such as preeclampsia and cytomegalovirus transmission.

KEYWORD

cytotrophoblast - vasculogenesis

REFERENCES

  • 1 Smith R. The timing of birth.  Sci Am . 1999;  280 68-75
    PubMedGoogle Scholar
  • 2 Brosens I, Dixon H G. The anatomy of the maternal side of the placenta.  J Obstet Gynaecol Br Commonw . 1966;  73 357-363
    PubMedGoogle Scholar
  • 3 Cross J C, Werb Z, Fisher S J. Implantation and the placenta: key pieces of the development puzzle.  Science . 1994;  266 1508-1518
    CrossrefPubMedGoogle Scholar
  • 4 Damsky C H, Fisher S J. Trophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors.  Curr Opin Cell Biol . 1998;  10 660-666
    CrossrefPubMedGoogle Scholar
  • 5 Damsky C H, Fitzgerald M L, Fisher S J. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo.  J Clin Invest . 1992;  89 210-222
    CrossrefPubMedGoogle Scholar
  • 6 Vicovac L, Jones C J, Aplin J D. Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro.  Placenta . 1995;  16 41-56
    CrossrefPubMedGoogle Scholar
  • 7 Blankenship T N, Enders A C. Expression of platelet-endothelial cell adhesion molecule-1 (PECAM) by macaque trophoblast cells during invasion of the spiral arteries.  Anat Rec . 1997;  247 413-419
    PubMedGoogle Scholar
  • 8 Zhou Y, Fisher S J, Janatpour M. Human cytotrophoblasts adopt a vascular phenotype as they differentiate: a strategy for successful endovascular invasion?.  J Clin Invest . 1997;  99 2139-2151
    CrossrefPubMedGoogle Scholar
  • 9 MacCalman C D, Furth E E, Omigbodun A, Bronner M, Coutifaris C, Strauss III F J. Regulated expression of cadherin-11 in human epithelial cells: a role for cadherin-11 in trophoblast-endometrium interactions?.  Dev Dyn . 1996;  206 201-211
    CrossrefPubMedGoogle Scholar
  • 10 Shih I M, Kurman R J. Expression of melanoma cell adhesion molecule in intermediate trophoblast.  Lab Invest . 1996;  75 377-388
    PubMedGoogle Scholar
  • 11 Burrows T D, King A, Loke Y W. Expression of adhesion molecules by endovascular trophoblast and decidual endothelial cells: implications for vascular invasion during implantation.  Placenta . 1994;  15 21-33
    PubMedGoogle Scholar
  • 12 Blankenship T N, King B F. Macaque intra-arterial trophoblast and extravillous trophoblast of the cell columns and cytotrophoblastic shell express neural cell adhesion molecule (NCAM).  Anat Rec . 1996;  245 525-531
    PubMedGoogle Scholar
  • 13 Pröll J, Blaschitz A, Hartmann M, Thalhamer J, Dohr G. Human first-trimester placenta intra-arterial trophoblast cells express the neural cell adhesion molecule.  Early Pregnancy . 1996;  2 271-275
    PubMedGoogle Scholar
  • 14 Starkey P M, Sargent I L, Redman C W. Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry.  Immunology . 1988;  65 129-134
    PubMedGoogle Scholar
  • 15 Librach C L, Werb Z, Fitzgerald M L. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts.  J Cell Biol . 1991;  113 437-449
    CrossrefPubMedGoogle Scholar
  • 16 Vu T H, Shipley J M, Bergers G. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes.  Cell . 1998;  93 411-422
    CrossrefPubMedGoogle Scholar
  • 17 Queenan J TJ, Kao L C, Arboleda C E. Regulation of urokinase-type plasminogen activator production by cultured human cytotrophoblasts.  J Biol Chem . 1987;  262 10903-10906
    PubMedGoogle Scholar
  • 18 Feinberg R F, Kao L C, Haimowitz J E. Plasminogen activator inhibitor types 1 and 2 in human trophoblasts: PAI-1 is an immunocytochemical marker of invading trophoblasts.  Lab Invest . 1989;  61 20-26
    PubMedGoogle Scholar
  • 19 Even-Ram S, Uziely B, Cohen P. Thrombin receptor overexpression in malignant and physiological invasion processes.  Nat Med . 1998;  4 909-914
    PubMedGoogle Scholar
  • 20 Clark D E, Smith S K, Licence D, Evans A L, Charnock-Jones D S. Comparison of expression patterns for placenta growth factor, vascular endothelial growth factor (VEGF), VEGF-B and VEGF-C in the human placenta throughout gestation.  J Endocrinol . 1998;  159 459-467
    CrossrefPubMedGoogle Scholar
  • 21 Nasu K, Zhou Y, McMaster M T, Fisher S J. Upregulation of human cytotrophoblast invasion by hepatocyte growth factor.  J Reprod Fertil . 2000;  (suppl 55) 73-80
    PubMedGoogle Scholar
  • 22 Ellis S A, Palmer M S, McMichael A J. Human trophoblast and the choriocarcinoma cell line BeWo express a truncated HLA class I molecule.  J Immunol . 1990;  144 731-735
    PubMedGoogle Scholar
  • 23 Kovats S, Main E K, Librach C, Stubblebine M, Fisher S J, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts.  Science . 1990;  248 220-223
    CrossrefPubMedGoogle Scholar
  • 24 Roth I, Corry D B, Locksley R M, Abrams J S, Litton M J, Fisher S J. Human placental cytotrophoblasts produce the immunosuppressive cytokine interleukin 10.  J Exp Med . 1996;  184 539-548
    CrossrefPubMedGoogle Scholar
  • 25 Burton G J, Jauniaux E, Watson A L. Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy: the Boyd collection revisited.  Am J Obstet Gynecol . 1999;  181 718-724
    CrossrefPubMedGoogle Scholar
  • 26 Genbacev O, Joslin R, Damsky C H, Polliotti B M, Fisher S J. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia.  J Clin Invest . 1996;  97 540-550
    CrossrefPubMedGoogle Scholar
  • 27 Genbacev O, Zhou Y, Ludlow J W, Fisher S J. Regulation of human placental development by oxygen tension.  Science . 1997;  277 1669-1672
    CrossrefPubMedGoogle Scholar
  • 28 Berg C J, Atrash H K, Koonin L M, Tucker M. Pregnancy-related mortality in the United States, 1987-1990.  Obstet Gynecol . 1996;  88 161-167
    CrossrefPubMedGoogle Scholar
  • 29 Levine R J, Hauth J C, Curet L B. Trial of calcium to prevent preeclampsia.  N Engl J Med . 1997;  337 69-76
    CrossrefPubMedGoogle Scholar
  • 30 Roberts J M, Taylor R N, Musci T J, Rodgers G M, Hubel C A, McLaughlin M K. Preeclampsia: an endothelial cell disorder.  Am J Obstet Gynecol . 1989;  161 1200-1204
    PubMedGoogle Scholar
  • 31 Ness R B, Roberts J M. Heterogeneous causes constituting the single syndrome of preeclampsia: a hypothesis and its implications.  Am J Obstet Gynecol . 1996;  175 1365-1370
    CrossrefPubMedGoogle Scholar
  • 32 Brosens I A, Robertson W B, Dixon H G. The role of the spiral arteries in the pathogenesis of preeclampsia.  Obstet Gynecol Annu . 1972;  1 177-191
    PubMedGoogle Scholar
  • 33 Zhou Y, Damsky C H, Chiu K, Roberts J M, Fisher S J. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts.  J Clin Invest . 1993;  91 950-960
    CrossrefPubMedGoogle Scholar
  • 34 Zhou Y, Damsky C H, Fisher S J. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype: one cause of defective endovascular invasion in this syndrome?.  J Clin Invest . 1997;  99 2152-2164
    CrossrefPubMedGoogle Scholar
  • 35 Robertson W B, Brosens I, Dixon G. Maternal uterine vascular lesions in the hypertensive complications of pregnancy.  Perspect Nephrol Hypertens . 1976;  5 115-127
    PubMedGoogle Scholar
  • 36 Fisher S, Genbacev O, Maidji E, Pereira L. Human cytomegalovirus infection of placental cytotrophoblasts in vitro and in utero: implications for transmission and pathogenesis.  J Virol . 2000;  74 6808-6820
    CrossrefPubMedGoogle Scholar
  • 37 Benirschke K, Mendoza G R, Bazeley P L. Placental and fetal manifestations of cytomegalovirus infection.  Virchows Arch B Cell Pathol . 1974;  16 121-139
    PubMedGoogle Scholar
  • 38 Boppana S B, Britt W J. Antiviral antibody responses and intrauterine transmission after primary maternal cytomegalovirus infection.  J Infect Dis . 1995;  171 1115-1121
    PubMedGoogle Scholar
  • 39 Britt W J. Congenital cytomegalovirus infection. In: Hitchcock PJ, MacKay HT, Wasserheit JN, eds. Sexually Transmitted Diseases and Adverse Outcomes of Pregnancy Washington, DC: ASM Press 1999: 269-281
    Google Scholar
  • 40 Chandler S H, Alexander E R, Holmes K K. Epidemiology of cytomegaloviral infection in a heterogeneous population of pregnant women.  J Infect Dis . 1985;  152 249-256
    PubMedGoogle Scholar
  • 41 Chandler S H, Handsfield H H, McDougall J K. Isolation of multiple strains of cytomegalovirus from women attending a clinic for sexually transmitted disease.  J Infect Dis . 1987;  155 655-660
    PubMedGoogle Scholar
  • 42 Chandler S H, Holmes K K, Wentworth B B. The epidemiology of cytomegaloviral infection in women attending a sexually transmitted disease clinic.  J Infect Dis . 1985;  152 597-605
    PubMedGoogle Scholar
  • 43 Coonrod D, Collier A C, Ashley R, DeRouen T, Corey L. Association between cytomegalovirus seroconversion and upper genital tract infection among women attending a sexually transmitted disease clinic: a prospective study.  J Infect Dis . 1998;  177 1188-1193
    PubMedGoogle Scholar
  • 44 Cross J C, Lam S, Yagel S, Werb Z. Defective induction of the transcription factor interferon-stimulated gene factor-3 and interferon alpha insensitivity in human trophoblast cells.  Biol Reprod . 1999;  60 312-321
    PubMedGoogle Scholar
  • 45 Damsky C H, Librach C, Lim K H. Integrin switching regulates normal trophoblast invasion.  Development . 1994;  120 3657-3666
    PubMedGoogle Scholar
  • 46 de Jong D M, Galasso G J, Gazzard B. Summary of the II International Symposium on Cytomegalovirus.  Antiviral Res . 1998;  39 141-162
    Google Scholar
  • 47 Dondero D V, Pereira L. Monoclonal antibody production. In: Emmons R, Schmidt N, eds. Diagnostic Procedures for Viral, Rickettsial and Chlamydial Infections Washington, DC: American Public Health Association 1990: 101-124
    Google Scholar
  • 48 Fisher S J, Cui T Y, Zhang L. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro.  J Cell Biol . 1989;  109 891-902
    CrossrefPubMedGoogle Scholar
  • 49 Fisher S J, Leitch M S, Kantor M S, Basbaum C B, Kramer R H. Degradation of extracellular matrix by the trophoblastic cells of first-trimester human placentas.  J Cell Biochem . 1985;  27 31-41
    CrossrefPubMedGoogle Scholar
  • 50 Fowler K B, Pass R F. Sexually transmitted diseases in mothers of neonates with congenital cytomegalovirus infection.  J Infect Dis . 1991;  164 259-264
    PubMedGoogle Scholar
  • 51 Fowler K B, Stagno S, Pass R F, Britt W J, Boll T J, Alford C A. The outcome of congenital cytomegalovirus infection in relation to maternal antibody status.  N Engl J Med . 1992;  326 663-667
    PubMedGoogle Scholar
  • 52 Furukawa T, Jisaki F, Sakamuro D, Takegami T, Murayama T. Detection of human cytomegalovirus genome in uterus tissue.  Arch Virol . 1994;  135 265-277
    CrossrefPubMedGoogle Scholar
  • 53 Genbacev O, Schubach S A, Miller R K. Villous culture of first trimester human placenta: model to study extravillous trophoblast (EVT) differentiation.  Placenta . 1992;  13 439-461
    PubMedGoogle Scholar
      >